Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice
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Abstract
Deciphering the genetic bases of behavioural traits is essential to understanding how they evolve and contribute to adaptation and biological diversification, but it remains a substantial challenge, especially for behavioural traits with polygenic architectures. In this study, we developed a population genomics approach coupled with functional predictions to address the evolution and genetic basis of olfactory-based assortative mate preferences in the house mouse, suspected to have evolved as a response to selection against hybridisation. We used whole genome resequencing data and the C2 statistic of the program BAYPASS, which contrasts allele frequencies corrected for population structure, to characterize genetic differentiation between sets of populations with strong contrast in behaviour (expressing or not assortative mate preferences) and we identified some regions of the genome showing the expected significant and consistent association with behavioural divergence. A series of Olfactory and Vomeronasal Receptor genes, among the most differentiated genomic regions and in line with functional predictions, stand out as the prime candidates underlying this olfactory-based behavioural divergence. These genes form large gene clusters in the genome, with two main candidate clusters extending up to 1.8 Mb. Variant analyses indicate a potential dual role of regulatory and protein-coding changes in the evolution of choosiness. This study shows that combining expectations on the genomic patterns of divergence with functional expectations represents a promising route to unravelling the genetic architecture of complex trait variation and provides novel insights into the role of olfactory and vomeronasal receptors in mammal adaptation and speciation.
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Differentiation-based genome scans lie at the core of speciation and adaptation genomics research. Dating back to Lewontin & Krakauer (1973), they have become very popular with the advent of genomics to identify genome regions of enhanced differentiation relative to neutral expectations. These regions may represent genetic barriers between divergent lineages and are key for studying reproductive isolation. However, genome scan methods can generate a high rate of false positives, primarily if the neutral population structure is not accounted for (Bierne et al. 2013). Moreover, interpreting genome scans can be challenging in the context of secondary contacts between diverging lineages (Bierne et al. 2011), because the coupling between different components of reproductive isolation (local adaptation, intrinsic incompatibilities, mating …
Differentiation-based genome scans lie at the core of speciation and adaptation genomics research. Dating back to Lewontin & Krakauer (1973), they have become very popular with the advent of genomics to identify genome regions of enhanced differentiation relative to neutral expectations. These regions may represent genetic barriers between divergent lineages and are key for studying reproductive isolation. However, genome scan methods can generate a high rate of false positives, primarily if the neutral population structure is not accounted for (Bierne et al. 2013). Moreover, interpreting genome scans can be challenging in the context of secondary contacts between diverging lineages (Bierne et al. 2011), because the coupling between different components of reproductive isolation (local adaptation, intrinsic incompatibilities, mating preferences, etc.) can occur readily, thus preventing the causes of differentiation from being determined.
Smadja and collaborators (2022) applied a sophisticated genome scan for trait association (BAYPASS, Gautier 2015) to underlie the genetic basis of a polygenetic behaviour: assortative mating in hybridizing mice. My interest in this neat study mainly relies on two reasons. First, the authors used an ingenious geographical setting (replicate pairs of “Choosy” versus “Non-Choosy” populations) with multi-way comparisons to narrow down the list of candidate regions resulting from BAYPASS. The latter corrects for population structure, handles cost-effective pool-seq data and allows for gene-based analyses that aggregate SNP signals within a gene. These features reinforce the set of outlier genes detected; however, not all are expected to be associated with mating preference.
The second reason why this study is valuable to me is that Smadja et al. (2022) complemented the population genomic approach with functional predictions to validate the genetic signal. In line with previous behavioural and chemical assays on the proximal mechanisms of mating preferences, they identified multiple olfactory and vomeronasal receptor genes as highly significant candidates. Therefore, combining genomic signals with functional analyses is a clever way to provide insights into the causes of reproductive isolation, especially when multiple barriers are involved. This is typically true for reinforcement (Butlin & Smadja 2018), suspected to occur in these mice because, in that case, assortative mating (a prezygotic barrier) evolves in response to the cost of hybridization (for example, due to hybrid inviability).
As advocated by the authors, their study paves the way for future work addressing the genetic basis of reinforcement, a trait of major evolutionary importance for which we lack empirical data. They also make a compelling case using complementary approaches that olfactory and vomeronasal receptors have a central role in mammal speciation.
References:Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20: 2044–2072. https://doi.org/10.1111/j.1365-294X.2011.05080.x
Bierne N, Roze D, Welch JJ (2013) Pervasive selection or is it…? why are FST outliers sometimes so frequent? Mol Ecol 22: 2061–2064. https://doi.org/10.1111/mec.12241
Butlin RK, Smadja CM (2018) Coupling, Reinforcement, and Speciation. Am Nat 191:155–172. https://doi.org/10.1086/695136
Gautier M (2015) Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates. Genetics 201:1555–1579. https://doi.org/10.1534/genetics.115.181453
Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of selective neutrality of polymorphisms. Genetics 74: 175–195. https://doi.org/10.1093/genetics/74.1.175
Smadja CM, Loire E, Caminade P, Severac D, Gautier M, Ganem G (2022) Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice. bioRxiv, 2022.07.21.500634, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.07.21.500634
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